Genetic Parentage in the Squat Lobsters Munida Rugosa and M

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Genetic Parentage in the Squat Lobsters Munida Rugosa and M Vol. 421: 173–182, 2011 MARINE ECOLOGY PROGRESS SERIES Published January 17 doi: 10.3354/meps08895 Mar Ecol Prog Ser Genetic parentage in the squat lobsters Munida rugosa and M. sarsi (Crustacea, Anomura, Galatheidae) Deborah A. Bailie, Rosaleen Hynes, Paulo A. Prodöhl* School of Biological Sciences, Queen’s University Belfast, Medical Biology Centre, 97 Lisburn Road, Belfast BT9 7BL, UK ABSTRACT: Munida is the most diverse and cosmopolitan genus of the galatheid squat lobsters. The group has attracted much attention in recent years from both systematic and evolutionary perspec- tives, yet information on the biology, ecology and evolution of this genus is very limited. We investi- gated the genetic parentage of 2 North Atlantic species, M. rugosa and M. sarsi, sampled from the Clyde Sea on the west coast of Scotland. Microsatellite markers were used to establish the parental contribution from embryos of berried females (M. rugosa, n = 25 and M. sarsi, n = 5). The frequency of multiple paternity observed in both species (86% for M. rugosa and 100% for M. sarsi) is the high- est ever reported for any marine crustaceans. Invariably more than 2 sires were involved in each case (minimum of 2 to 3 for M. rugosa and 4 for M. sarsi). Our findings indicate that multiple paternity is likely to be the norm in both species. Within most multiply sired broods, sire contribution was highly skewed towards a single male (66% of broods for M. rugosa and 100% for M. sarsi). Furthermore, embryos from different sires were randomly distributed across the female’s brood patch. This is the first report of multiple paternity in galatheids. While a number of theories can account for the high incidence of multiple paternity in these species (e.g. convenience polyandry as a result of cryptic female choice, forced copulations, the influence of fishing pressures), at present it is not possible to disentangle their individual and/or combined effects. KEY WORDS: Galatheids · Crustacean mating system · Polyandry · Munida spp. Resale or republication not permitted without written consent of the publisher INTRODUCTION (Sainte-Marie et al. 1997), convenience polyandry (Thiel & Hinojosa 2003) and cryptic female choice The mating behaviour of decapod crustaceans has (Walker et al. 2002, Thiel & Hinojosa 2003). received considerable attention in recent years (re- A major difficulty in examining the mating behav- viewed by Correa & Thiel 2003, Duffy & Thiel 2007). iour of marine crustaceans in general is associated with Many studies have elaborated on male mating behav- the obvious logistical difficulties of observing mating iours such as mate guarding and aggression (Wada et interactions in their natural environment. The elusive al. 1997, Jivoff & Hines 1998, Rondeau & Sainte-Marie burrowing behaviour and/or nocturnal activities of 2001), or sperm competition. The latter has focused on many species (De Grave & Turner 1997) further com- sperm stratification (Urbani et al. 1998), removal plicate studies on mating. While laboratory experi- (Beninger et al. 1991) and/or limitation (MacDiarmid & ments have contributed to a better understanding of Butler 1999, Rondeau & Sainte-Marie 2001, Rubolini et the mating behaviour of some species (e.g. Urbani et al. 2005). More recently, attention has shifted towards al. 1998, Thiel & Hinojosa 2003), the mating systems of the examination of female behaviour. These studies the majority of crustaceans are still poorly understood. have addressed questions related to mate selection Molecular studies are now providing a powerful alter- *Corresponding author. Email: [email protected] © Inter-Research 2011 · www.int-res.com 174 Mar Ecol Prog Ser 421: 173–182, 2011 native for investigating the mating strategies of other- cephalothorax, forming a spawning chamber where wise elusive and/or difficult target species (e.g. eggs are brooded until they hatch. It is not known Bilodeau et al. 2005) whether a female can mate with more than 1 male dur- Molecular investigations of paternity among marine ing a breeding season. While the timing of reproduc- crustaceans are still rare in comparison with other tion is unclear for M. sarsi, in western Scotland M. taxa. With a few exceptions, focusing on brachyuran rugosa produce broods from November, with hatching crabs (Urbani et al. 1998, McKeown & Shaw 2008), the occurring from March to May (Lebour 1930, Zainal majority of other studies on marine crustaceans have 1990, Coombes 2002). Extruded broods contain up to reported on the incidence of multiple paternity, e.g. ~32 000 eggs which are approximately 0.5 mm in porcelain crab Petrolisthes cinctipes (Toonen 2004), diameter (Wenner 1982, Tapella et al. 2002). crayfish Orconectes placidus (Walker et al. 2002), Other crustacean species displaying mating behav- American lobster Homarus americanus (Gosselin et iour similar to squat lobsters, including forced copula- al. 2005) and ghost shrimp Callichirus islagrande tion (e.g. crayfish) and lack of sperm storage structures (Bilodeau et al. 2005). Knowledge of mating strategies (e.g. rock shrimp), are characterised by multiple mat- is particularly relevant for species subject to intense ing. While it is still unknown as to whether multiple fishing exploitation. For instance, in the American lob- mating behaviour translates into multiple genetic ster, Gosselin et al. (2005) showed that mating strate- paternity in rock shrimp, this has been confirmed for gies can vary geographically in correlation with differ- crayfish (Walker et al. 2002). Thus, we hypothesised ent levels of exploitation. The authors suggested that that genetic multiple paternity is the mating strategy of selective fishing pressure for large males could be the galatheid species investigated. In order to test this responsible for such a pattern. hypothesis in Munida rugosa and M. sarsi, we gener- Munida is the most diverse and cosmopolitan genus ated and compared microsatellite multilocus geno- of the galatheid squat lobsters and, as such, has types of females and their egg broods in order to attracted much attention in recent years from both a deduce paternal contribution. systematic and evolutionary perspective. However, information regarding the biology, ecology and evolu- tion of this genus is still limited. Munida rugosa and M. MATERIALS AND METHODS sarsi are endemic to the north-eastern Atlantic. They inhabit rocky or soft mud substrata in shelf waters Study sites and collections. Given their elusive ranging from the shallow to the deeper continental nature and habitat preferences (individuals often bury slope. Similar to other Munida species, M. rugosa and themselves in muddy substrata), it is notoriously diffi- M. sarsi are gonochoric, but little is known about the cult to study the mating behaviour of these species in mating behaviour of these species. They are benthic as their natural environment. This is particularly the case adults with a planktotrophic larval phase and a devel- for egg-carrying females, making them very hard to opmental period that lasts 3 to 4 mo (Schmidt 1965, obtain. Indeed, at least for Munida rugosa, fisheries Gore 1979, Van Dover & Williams 1991). Clarification have been reported to be biased towards males of the mating system of Munida species is now of par- (Coombes 2002). Furthermore, in comparison to M. ticular relevance not only because of the increasing rugosa, M. sarsi, as the deeper water species, is consid- target fisheries, but also due to the impact from indi- erably more difficult to sample. Thus, despite consider- rect fishing pressures. In western Scotland, for able effort, sampling success for ovigerous females instance, M. rugosa comprises a large component of was limited. M. rugosa (n = 25) and M. sarsi (n = 5) bycatch from the large-scale commercial Nephrops ovigerous females were collected by a 2 m beam trawl norvegicus fisheries (Bergmann & Moore 2001). using a 50 mm mesh in the Clyde Sea (western Scot- Pothanikat (2005) produced the only report detailing land) in March 2005 and February 2006. The abdomen the mating behaviour of Munida sarsi, which was and associated eggs from each female were stored in based upon laboratory observations. The report stated 99% molecular grade ethanol for subsequent analysis. that coerced mating occurs in the hard-shelled state, Species identification was confirmed by genetic with a male holding a female in place with his che- screening using diagnostic mtDNA markers (Bailie lipeds, while trying to insert a spermatophore into the 2008). abdominal area of the female with the help of his fifth DNA extraction and amplification of microsatel- pereiopods. Females possess no internal organs for lites. Genomic DNA was extracted from the muscle tis- sperm storage, and there is no information as to how sue of the ovigerous females as described by Taggart the female handles the spermatophore or how egg et al. (1992). For Munida rugosa samples, 11 eggs were insemination takes place. Following insemination, randomly collected from each of the 4 pleopodal however, the female’s abdomen is cupped under the regions (totalling 44 eggs female–1). A similar sampling Bailie et al.: Multiple paternity in Munida spp. 175 strategy was carried out for M. sarsi, except that 23 loaded into a 25 cm 6% 1× TBE polyacrylamide gel us- eggs were randomly removed from each of the 3 ing a commercially available size-standard ladder for the pleopodal regions (totalling 69 eggs female–1). This Li-Cor system (Microstep-13a/b and 20a, Microzone) to sequential egg sampling strategy (i.e. obtaining sam- accurately estimate the size of allelic fragments. Gels ples from all pleopodal regions) was carried out in were run on the Li-Cor system at a constant power of order to account for any potential variation in the tim- 40 W at a temperature of ~50°C for 1 to 2 h. Genotypic ing or order of egg extrusion by females. DNA egg scoring was carried out using the computer software extraction was carried out using a standard Chelex Gene Profiler (Scanalytics). extraction protocol using a 96-well format microtitre Statistical analysis.
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